Neutering

Neutering, from the Latin neuter ("of neither sex"^[1]), is the removal of an animal's reproductive organ, either all of it or a considerably large part. "Neutering" is often used incorrectly to refer only to male animals, but the term actually applies to both sexes. The male-specific term is castration, while spaying is usually reserved for female animals. Colloquially, both terms are often referred to as fixing.^[2] In male horses, castrating is referred to as gelding. Modern veterinary practice tends to use the term "de-sexing".

Neutering is the most common method for the sterilization of animals. In the United States, most humane societies, animal shelters, and rescue groups urge pet owners to have their pets neutered to prevent the births of unwanted litters, which contribute to the overpopulation of unwanted animals in the rescue system. Many states require that all adopted cats, kittens, dogs, and puppies be sterilized before going to their new homes.

The practice has been advocated in radio and television commercials and on various shows, most notably the game show The Price is Right, whose host, Bob Barker, would end every episode with the catchphrase "Help control the pet population; have your pets spayed or neutered." After Barker's retirement, Drew Carey continued to sign off with his own message regarding spaying and neutering.

Health and behavioral effects

Advantages

Besides being a birth control method, and being convenient to many owners, castrating/spaying has the following health benefits:

• Sexually dimorphic behaviors such as mounting, urine spraying and some forms of male aggression are reduced due to the decrease in hormone levels brought about by neutering. This is especially significant in male cats due to the extreme undesirability of these male cat sexual behaviors for many pet owners.^[3]
• Early spaying significantly reduces the risk of development of mammary tumours in dogs. The incidence of mammary tumours in un-spayed female dogs is 71% (of which approximately 50% will be malignant and 50% will be benign), but if a dog is spayed before its first season, the risk of developing a mammary tumour is reduced to 0.35%—a 99.5% reduction. The positive effects of spaying on reduction of later mammary tumours decreases with each season the dog has (backing up the contention that the greatest benefit to reduce future mammary tumour development is to spay before the first season), and there is no added benefit to spaying to reduce recurrence of a mammary tumour once it has been diagnosed.^[4]
• Neutering increases life expectancy in cats: one study found castrated male cats live twice as long as intact males, while spayed female cats live 62% longer than intact females. Non-neutered cats in the USA are three times more likely to require treatment for an animal bite.Having a cat neutered confers health benefits, because castrated males cannot develop testicular cancer, spayed females cannot develop uterine, cervical or ovarian cancer, and both have a reduced risk of mammary cancer.
• Without the ability to reproduce, a female necessarily has zero risk of pregnancy complications, such as spotting and false pregnancy, the latter of which can occur in more than 50% of unspayed female dogs.^[5]
• Pyometra, uterine cancer, ovarian cancer, and testicular cancer are prevented, as the susceptible organs are removed, though stump pyometra may still occur in spayed females.
• Pyometra (or a pus filled womb) ('Pyo' = pus; 'metra' = uterus or womb) is a life-threatening condition that requires emergency veterinary treatment. The risk of an entire bitch developing pyometra by age 10 is 25% across all breeds, but can be as high as 54% in some breeds.^[6] The treatment of choice for a closed-pyometra (where the cervix is closed and the pus cannot drain) is admission to hospital, commencement on intravenous fluids and appropriate antibiotics and, once stable enough for the anaesthetic and surgery, emergency removal of the infected pus-filled uterus. Medical management can be attempted if the animal's condition allows (for example in the case of an 'open' pyometra where the pus drains per-vaginum from the uterus via the open cervix) or dictates (where the animal is too old or otherwise unwell to withstand surgery), if the owner wishes to keep the dog entire to breed or if the owner is unable to afford the veterinary fees associated with surgery. Emergency removal of the infected uterus carries a much higher degree of risk of death than a routine 'spay' operation. The risk of death from in dogs undergoing surgical treatment for pyometra is up to 17%.^[7] Thus the risk of death in entire female dogs from a pyometra, even if given correct veterinary attention can be up to 9% by 10 years of age (17% of 54%). This risk is reduced to virtually zero if spayed.

Disadvantages

General

• As with any surgical procedure, immediate complications of neutering include the usual anesthetic and surgical complications, such as bleeding, infection, and death. These risks are relatively low in routine neutering; however, they may be increased for some animals due to other pre-existing health factors. In one study the risk of anesthetic-related death (not limited to neutering procedures) was estimated at 0.05% for healthy dogs and 0.11% for healthy cats. The risks for sick animals were 1.33% for dogs and 1.40% for cats.^[8]
• Spaying and castrating cats and dogs may increase the risk of obesity if nutritional intake is not reduced to reflect the lower metabolic requirements of neutered animals.^[9] In cats, a decrease in sex hormone levels seems to be associated with an increase in food intake.^[10] In dogs, the effects of neutering as a risk factor for obesity vary between breeds.^[11]
• Neutered dogs of both sexes are at a twofold excess risk to develop osteosarcoma (bone cancer) as compared to intact dogs. The risk of osteosarcoma increases with increasing breed size and especially height.^[12][13][14]
• Studies of cardiac tumors in dogs showed that there was a 5 times greater risk of hemangiosarcoma (cancer of blood vessel lining), one of the three most common cancers in dogs, in spayed females than intact females and a 2.4 times greater risk of hemangiosarcoma in castrated dogs as compared to intact males.^[15][16]
• Spaying and castrating is associated with an increase in urinary tract cancers in dogs, however the risk is still less than 1%.^[17]
• Neutered dogs of both sexes have a 27% to 38% increased risk of adverse reactions to vaccinations. However, the incidence of adverse reactions for neutered and intact dogs combined is only 0.32%.^[18]
• Neutered dogs have also been known to develop hormone-responsive alopecia (hair loss).^[19]
• A 2004 study found that neutered dogs had a higher incidence of cranial cruciate ligament (CCL) rupture, a form of anterior cruciate ligament (ACL) injury.^[20]
• A study of golden retrievers found that castrated males were 3 times more likely than intact males to be diagnosed with lymphoma and 2 times more likely to have hip dysplasia.^[21]

Specific to males

• About 2% of castrated male dogs eventually develop prostate cancer, compared to less than 0.6% of intact males.^[22][23] The evidence is most conclusive for Bouviers.^[17]
• In a study of 29 intact male dogs and 47 castrated males aged 11–14, the neutered males were significantly more likely to progress from one geriatric cognitive impairment condition (out of the four conditions – disorientation in the house or outdoors, changes in social interactions with human family members, loss of house training, and changes in the sleep-wake cycle) to two or more conditions. Testosterone in intact males is thought to slow the progression of cognitive impairment, at least in dogs that already have mild impairment.^[24]
• As compared to intact males, castrated cats are at an increased risk for certain problems associated with feline lower urinary tract disease, including the presence of stones or a plug in the urethra and urethral blockage.^[25]
• Neutering also has been associated with an increased likelihood of urethral sphincter incontinence in male dogs.^[26]

Specific to females

• There is some weak evidence that spaying can increase the risk of urinary incontinence in dogs, especially when done before the age of three months. Up till 12 months of age, the risk decreases as the age at spaying increases.^[27]
• Spayed female dogs are at an increased risk of hypothyroidism.^[28]

Current research

Various studies of the effects neutering has overall on male and female dog aggression have been unable to arrive at a consensus. A possible reason for this according to two studies is changes to other factors have more of an effect than neutering.^[29][30] One study reported results of aggression towards familiar and strange people and other dogs reduced between 10 and 60 percent of cases,^[31] while other studies reported increases in possessive aggression^[32] and aggression towards familiar and strange people,^[33] and more studies reported there was no significant difference in aggression risk between neutered and non-neutered males.^[30][34] For females with existing aggression, many studies reported increases in aggressive behavior^{[35][36][37][38]} and some found increased separation anxiety behavior.^[33][39] A report from the American Kennel Club Canine Health Foundation reported significantly more behavioral problems in castrated dogs. The most commonly observed behavioral problem in spayed females was fearful behavior and the most common problem in males was aggression.^[40] Early age gonadectomy is associated with an increased incidence of noise phobias and undesirable sexual behaviors.^[41]

Methods of sterilization

Females (spaying)

Feline uterus

In female animals, spaying involves abdominal surgery to remove the ovaries and uterus (hystero-oophorectomy). Another option is to remove only the ovaries (oophorectomy), which is mainly done in cats and young dogs, and yet another, less commonly performed method is an "ovary sparing spay" in which the uterus is removed but one (or both) ovaries are left. Traditional spaying (removal of uterus and ovaries) is performed commonly on household pets (such as cats and dogs), as a method of birth control. It is performed less commonly on livestock, as a method of birth control or for other reasons. In mares, these other reasons include behavior modification.^[42]

Surgical incision site of a female cat

The surgery can be performed using a traditional open approach or by laparoscopic "keyhole" surgery. Open surgery is more widely available as laparoscopic surgical equipment costs are expensive.

Traditional open surgery is usually performed through a ventral midline incision below the umbilicus. The incision size varies depending upon the surgeon and the size of the animal. The uterine horns are identified and the ovaries are found by following the horns to their ends.

There is a ligament that attaches the ovaries to the body wall, which may need to be broken down so the ovaries can be identified. The ovarian arteries are then ligated with resorbable suture material and then the arteries transected. The uterine body (which is very short in litter-bearing species) and related arteries are also tied off just in front of the cervix (leaving the cervix as a natural barrier). The entire uterus and ovaries are then removed. The abdomen is checked for bleeding and then closed with a three-layer closure. The linea alba and then the subcutaneous layer are closed with resorbable suture material. The skin is then stapled, sutured, or glued closed.

Laparoscopic surgery is performed using a camera and instruments placed through small incisions (ports) in the body wall. The patient is under anaesthesia and lying on the back. The incisions are between 5 and 10 millimetres (0.20 and 0.39 in) and the number varies according to the equipment and technique used. The surgeon watches on a screen during the operation. The first port is made just behind the umbilicus and the camera is inserted. The abdomen is inflated with carbon dioxide gas to create a space to operate in. A second port is introduced a few centimeters in front of the navel and a long grasping instrument called a Babcock forceps is inserted. The surgeon finds the ovary with the instrument and uses it to suspend the ovary from a needle placed through the abdominal wall. This lifts the ovary and uterus safely away from other organs. The surgeon then removes the grasping instrument and replaces it with an instrument that cauterizes and cuts tissue. This instrument uses electricity to heat the blood vessels to seal them and to cut them. No sutures are placed inside. The ovary is separated from the uterus and round ligament. The cautery instrument is removed and replaced by the grasping instrument, which is used to pull the ovary out through the small abdominal incision (port). This is repeated on the other side and the small holes are closed with a few sutures.

The benefits of laparoscopic surgery are less pain, faster recovery, and smaller wounds to heal. A study has shown that patients are 70% more active in the first three days post-surgery compared to open surgery. The reason open surgery is more painful is that larger incisions are required, and the ovary needs to be pulled out of the body, which stretches and tears tissue in the abdomen (it is not uncommon for patients to react under anaesthesia by breathing faster at this point).

Spaying in female dogs removes the production of progesterone, which is a natural calming hormone and a serotonin uplifter. Spaying may therefore escalate any observable aggressive behaviour, either to humans or other dogs.^{[35][36][37][38]}

The risk of infections, bleeding, ruptures, inflammation and reactions to the drugs given to the animal as part of the procedure are all possibilities that should be considered.

Males (castration or vasectomy)

In male animals, castration involves the removal of the testes, and is commonly practiced on both household pets (for birth control and behaviour modification) and on livestock (for birth control, as well as to improve commercial value).

Nonsurgical alternatives

Injectable

• Male animals – Injecting a solution of calcium chloride dihydrate (20% by weight of CaCl₂ dissolved in ethanol – 95% ABV) into the testes of the animal results in nonsurgical castration. Within one month, necrosis of the testicular tissue causes sterilization.^[43][44]
• Male dogs – Neutersol (Zinc gluconate neutralized by arginine). Cytotoxic; produces irreversible infertility by chemical disruption of the testicle. It is now produced as Esterilsol in Mexico.^[45]
• Male rats – Adjudin (analogue of indazole-carboxylic acid), induces reversible germ cell loss from the seminiferous epithelium by disrupting cell adhesion function between nurse cells and immature sperm cells, preventing maturation.
• Male mice – injection of a solution of the JQ1 molecule to bind to a pocket of BRDT necessary for chromatin remodeling, which gives the proteins that regulate how genes act access to the genetic material^[46]
• Male sheep and pigs – Wireless Microvalve.^[47] Using a piezoelectric polymer that will deform when exposed to a specific electric field broadcast from a key fob (like a car alarm) the valve will open or close, preventing the passage of sperm, but not seminal fluid. Located in a section of the vas deferens that occurs just after the epididymis, the implantation can be carried out by use of a hypodermic needle.
• Female mammals – Vaccine of antigens (derived from purified Porcine zona pellucida) encapsulated in liposomes (cholesterol and lecithin) with an adjuvant, latest US patent RE37,224 (as of 2006-06-06), CA patent 2137263 (issued 1999-06-15). Product commercially known as SpayVac,^[48] a single injection causes a treated female mammal to produce antibodies that bind to ZP3 on the surface of her ovum, blocking sperm from fertilizing it for periods from 22 months up to 7 years (depending on the animal^[49][50]). This will not prevent the animal from going into heat (ovulating) and other than birth control, none of the above-mentioned advantages or disadvantages apply.

Other

• Male mammal – Noninvasive vasectomy using ultrasound.^[51]
• Male mice – reversible regulation of the KATNAL1 gene in Sertoli Cell Microtubule Dynamics of the testes.^[52]
• Female mammals – orally administered phosphodiesterase 3 inhibitor ORG 9935 daily before and during ovulation, which blocks the resumption of meiosis resulting in ovulation of a non-fertilizable, immature oocyte without rupturing the follicle.^[53]

Surgical alternatives

Vasectomy: The cutting and tying of the vasa deferentia. Failure rates are insignificantly small. This procedure is routinely carried out on male ferrets and sheep to manipulate the estrus cycles of in-contact females. It is uncommon in other animal species.

Tubal Ligation: Snipping and tying of fallopian tubes as a sterilization measure can be performed on female cats and dogs. Risk of unwanted pregnancies is insignificantly small. Only a few veterinarians will perform the procedure.

Like other forms of neutering, vasectomy and tubal ligation eliminate the ability to produce offspring. They differ from neutering in that they leave the animal's levels and patterns of sex hormone unchanged. Both sexes will retain their normal reproductive behavior, and other than birth control, none of the advantages and disadvantages listed above apply. This method is favored by some people who seek minimal infringement on the natural state of companion animals to achieve the desired reduction of unwanted births of cats and dogs.

Penile translocation is sometimes performed in cattle to produce a "teaser bull", who retains his full libido, but is incapable of intromission. This is done to identify estrous cows without the risk of transmitting venereal diseases.^[54]

Early-age neutering

Early-age neutering, also known as pediatric spaying or prepubertal gonadectomy, is the removal of the ovaries or testes before the onset of puberty. It is used mainly in animal sheltering and rescue where puppies and kittens can be neutered before being adopted out, eliminating non-compliance with sterilization agreement, which is typically above 40%.^[3] The American Veterinary Medical Association, American Animal Hospital Association and the Canadian Veterinary Medical Association support the procedure for population control, provided that the veterinarian uses his/her best knowledge when making the decision about the age at neutering.^[55][56][57]

While the age-unrelated risks and benefits cited above also apply to early-age neutering, various studies have indicated that the procedure is safe and not associated with increased mortality or serious health and behavioral problems when compared to conventional age neutering.^{[58][59][60][61][62]} Anesthesia recovery in young animals is usually more rapid and there are fewer complications.^[62][63] One study found that in female dogs there is an increasing risk of urinary incontinence the earlier the procedure is carried out; the study recommended that female dogs be spayed no earlier than 3 to 4 months of age.^[59] A later study comparing female dogs spayed between 4 to 6 months and after 6 months showed no increased risk.^[64]

One study showed the incidence of hip dysplasia increased to 6.7% for dogs neutered before 5.5 months compared to 4.7% for dogs neutered after 5.5 months, although the cases associated with early age neutering seems to be of a less severe form. There was no association between age of neutering and arthritis or long-bone fractures.^[59] Another study showed no correlation between age of neutering and musculoskeletal problems.^[61] A study of large breed dogs with cranial cruciate ligament rupture associated early-age neutering with the development of an excessive tibial plateau angle.^[65]

Of particular note are two recent studies from Lynette Hart's lab at UC Davis,^[66] as of 2015 the highest ranking veterinary institution in the US.^[67] The first study from 2013, published in a well-known interdisciplinary peer-reviewed journal ^[68] demonstrated "no cases of CCL (cruciate ligament tear) diagnosed in intact males or females, but in early-neutered males and females the occurrences were 5 percent and 8 percent, respectively. Almost 10 percent of early-neutered males were diagnosed with LSA (lymphosarcoma), 3 times more than intact males. The percentage of HSA (hemangiosarcoma) cases in late-neutered females (about 8 percent) was 4 times more than intact and early-neutered females. There were no cases of MCT (mast cell tumor) in intact females, but the occurrence was nearly 6 percent in late-neutered females"

The second study from 2014 ^[69] highlighted significant difference in closely related breeds (retrievers), suggesting that inter-breed variability is quite high and that sweeping legal measures and surgical mandates are not the best solutions to canine welfare and health. Specifically the study states: "In Labrador Retrievers, where about 5 percent of gonadally intact males and females had one or more joint disorders, neutering at 6 months doubled the incidence of one or more joint disorders in both sexes. In male and female Golden Retrievers, with the same 5 percent rate of joint disorders in intact dogs, neutering at 6 months increased the incidence of a joint disorder to 4–5 times that of intact dogs. The incidence of one or more cancers in female Labrador Retrievers increased slightly above the 3 percent level of intact females with neutering. In contrast, in female Golden Retrievers, with the same 3 percent rate of one or more cancers in intact females, neutering at all periods through 8 years of age increased the rate of at least one of the cancers by 3–4 times. In male Golden and Labrador Retrievers neutering had relatively minor effects in increasing the occurrence of cancers."

In terms of behavior in dogs, separation anxiety, aggression, escape behavior and inappropriate elimination are reduced while noise phobia and sexual behavior was increased. In males with aggression issues, earlier neutering may increase barking.^[59] In cats, asthma, gingivitis, and hyperactivity were decreased, while shyness was increased. In male cats, occurrence of abscesses, aggression toward veterinarians, sexual behaviors, and urine spraying was decreased, while hiding was increased.^[58]

Terminology for neutered animals

Male animals

Neutered (castrated) males of given animal species sometimes have specific names:

• Dog
• Cat, ferret – Gib
• Cattle – Bullock, Ox, Steer, Stag
• Chicken – Capon
• Deer – Havier
• Goat – Wether
• Horse, Donkey – Gelding
• Pig – Barrow
• Rabbit – Lapin
• Sheep – Wether

Female animals

A specialized vocabulary in animal husbandry and fancy has arisen for neutered (spayed) females of given animal species:

• Chicken – Poulard
• Ferret – Sprite

Religious views on neutering

Islam

While there are differing views in Islam with regard to neutering animals,^[70] some Islamic associations have stated that when done to maintain the health and welfare of both the animals and the community, neutering is allowed on the basis of 'maslaha' (general good)^[71] or "choos[ing] the lesser of two evils".^[72]

Judaism

Orthodox Judaism forbids the castration of both humans and non-human animals by Jews,^[73] except in lifesaving situations.^[74] In 2007, the Sephardic Chief Rabbi of Israel Rabbi Shlomo Amar issued a ruling stating that it is permissible to have companion animals neutered on the basis of the Jewish mandate to prevent cruelty to animals.^[75]

See also

• AB 1634 – A California bill proposing mandatory neuter laws.
• Animal population control
• Animal shelter
• Forced sterilization
• Hysterectomy
• Oophorectomy
• Overpopulation in companion animals
• Spay Day USA
• Wildlife contraceptive

References

1. University of Notre Dame online Latin dictionary
2. "Fix" at Merriam-Webster.com
3. Kustritz, Margaret V. Root (2007). "Determining the Optimal age for Gonadectomy of Dogs and Cats". Journal of the American Veterinary Medical Association 231 (11): 1665–75. doi:10.2460/javma.231.11.1665. PMID 18052800.
4. Poulton, Gerry. "Mammary Tumours in Dogs" (PDF). Irish Veterinary Journal.
5. Gobello, C.; et al. (23 August 2001). "Canine Pseudopregnancy: A Review" (PDF). IVIS.org. International Veterinary Information Service. Retrieved 13 April 2010.
6. "Breed Risk of Pyometra in Insured Dogs in Sweden". Journal of Veterinary Internal Medicine 15: 530–538. doi:10.1111/j.1939-1676.2001.tb01587.x.
7. "Results and complications of surgical treatment of pyometra: a review of 80 cases". Journal of the American Animal Hospital Association.
8. Brodbelt; Blissitt, K. J.; Hammond, R. A.; Neath, P. J.; Young, L. E.; Pfeiffer, D. U.; Wood, J. L. (2008). "The risk of death: the confidential enquiry into perioperative small animal fatalities". Veterinary Anaesthesia and Analgesia 35 (5): 365–73. doi:10.1111/j.1467-2995.2008.00397.x. PMID 18466167.
9. Colliard L.; Paragon B. M.; Lemuet B.; Bénet J. J.; Blanchard G. (February 2009). "Prevalence and risk factors of obesity in an urban population of healthy cats". J. Feline Med. Surg. 11 (2): 135–40. doi:10.1016/j.jfms.2008.07.002. PMID 18774325.
10. Cave N. J.; Backus R. C.; Marks S. L.; Klasing K. C. (October 2007). "Oestradiol, but not genistein, inhibits the rise in food intake following gonadectomy in cats, but genistein is associated with an increase in lean body mass". J Anim Physiol Anim Nutr (Berl) 91 (9–10): 400–10. doi:10.1111/j.1439-0396.2006.00667.x. PMID 17845247.
11. McGreevy P. D.; Thomson P. C.; Pride C.; Fawcett A.; Grassi T.; Jones B. (May 2005). "Prevalence of obesity in dogs examined by Australian veterinary practices and the risk factors involved". Vet. Rec. 156 (22): 695–702. doi:10.1136/vr.156.22.695. PMID 15923551.
12. Priester; McKay, F. W. (1980). "The Occurrence of Tumors in Domestic Animals". National Cancer Institute monograph (54): 1–210. PMID 7254313.
13. Ru, G.; Terracini, B.; Glickman, L. (1998). "Host related risk factors for canine osteosarcoma". The Veterinary Journal 156 (1): 31–9. doi:10.1016/S1090-0233(98)80059-2. PMID 9691849.
14. Cooley, D. M.; Beranek, B. C.; et al. (1 November 2002). "Endogenous gonadal hormone exposure and bone sarcoma risk". Cancer Epidemiol Biomarkers Prev 11 (11): 1434–40. PMID 12433723.
15. Prymak C.; McKee L. J.; Goldschmidt M. H.; Glickman L. T. (1988). "Epidemiologic, clinical, pathologic, and prognostic characteristics of splenic hemangiosarcoma and splenic hematoma in dogs: 217 cases (1985)". J Am Vet Med Assoc 193 (6): 706–712. PMID 3192450.
16. Ware, Wendy A.; Hopper, David L. (1999). "Cardiac Tumors in Dogs: 1982–1995". Journal of Veterinary Internal Medicine 13 (2): 95–103. doi:10.1892/0891-6640(1999)013<0095:CTID>2.3.CO;2. PMID 10225598.
17. Sanborn, L. J. (14 May 2007). "Long-Term Health Risks and Benefits Associated with Spay / Neuter in Dogs" (PDF). Retrieved 13 April 2010.
18. Moore G. E.; Guptill L. F.; Ward M. P.; Glickman N. W.; Faunt K. F.; Lewis H. B.; Glickman L.T. (2005). "Adverse events diagnosed within three days of vaccine administration in dogs". J Am Vet Med Assoc 227 (7): 1102–1108. doi:10.2460/javma.2005.227.1102. PMID 16220670.
19. Ettinger, Stephen J.; Feldman, Edward C. (1995). Textbook of Veterinary Internal Medicine (4th ed.). W. B. Saunders Company. ISBN 0-7216-6795-3.
20. Slauterbeck, J. R.; Pankratz, K.; Xu, K. T.; Bozeman, S. C.; Hardy, D. M. (Dec 2004). "Canine Ovariohysterectomy and Orchiectomy Increases the Prevalence of ACL Injury". Clinical Orthopaedics and Related Research 429: 301–5. doi:10.1097/01.blo.0000146469.08655.e2.
21. Torres de la Riva, Gretel. "Neutering Dogs: Effects on Joint Disorders and Cancers in Golden Retrievers". PLOS ONE 8: e55937. doi:10.1371/journal.pone.0055937.
22. Teske, E.; Naan, E. C.; Van Dijk, E. M.; Van Garderen, E.; Schalken, J. A. (2002). "Canine prostate carcinoma: epidemiological evidence of an increased risk in castrated dogs". Molecular and Cellular Endocrinology 197 (1–2): 251–5. doi:10.1016/S0303-7207(02)00261-7. PMID 12431819.
23. Sorenmo, K. U.; Goldschmidt, M.; Shofer, F.; Goldkamp, C.; Ferracone, J. (2003). "Immunohistochemical characterization of canine prostatic carcinoma and correlation with castration status and castration time". Veterinary and Comparative Oncology 1 (1): 48–56. doi:10.1046/j.1476-5829.2003.00007.x. PMID 19379330.
24. Hart (2001). "Effect of gonadectomy on subsequent development of age-related cognitive impairment in dogs". Journal of the American Veterinary Medical Association 219 (1): 51–6. doi:10.2460/javma.2001.219.51. PMID 11439769.
25. Lekcharoensuk; Osborne, C. A.; Lulich, J. P. (2001). "Epidemiologic study of risk factors for lower urinary tract diseases in cats". Journal of the American Veterinary Medical Association 218 (9): 1429–35. doi:10.2460/javma.2001.218.1429. PMID 11345305.
26. Aaron, A.; Eggleton, K.; Power, C.; Holt, P. E. "Urethral sphincter mechanism incompetence in male dogs: a retrospective analysis of 54 cases". Vet Rec. 139 (542-6): 1996.
27. Beauvais, W.; Cardwell, J. M.; Brodbelt, D. C. (2012). "The effect of neutering on the risk of urinary incontinence in bitches - a systematic review". Journal of Small Animal Practice 53 (4): 198–204. doi:10.1111/j.1748-5827.2011.01176.x. PMID 22353203.
28. Panciera D. L. (1994). "Hypothyroidism in dogs: 66 cases (1987–1992)". J Amer Vet Med Assoc 204 (5): 761–767.
29. Kobelt A. J.; Hemsworth P. H.; Barnett J. L.; Coleman G. J. (2003). "A survey of dog ownership in suburban Australia-conditions and behaviour problems". Appl. Anim. Behav. Sci. 82 (2): 137–148. doi:10.1016/S0168-1591(03)00062-5.
30. Casey R. A.; Loftus B.; Bolster C.; Richards G. J.; Blackwell E. J. (March 2014). "Human directed aggression in domestic dogs (Canis familiaris): Occurrence in different contexts and risk factors". Appl. Anim. Behav. Sci. 152: 52–63. doi:10.1016/j.applanim.2013.12.003.
31. The Effects of Spaying and Neutering on Canine Behavior James O’Heare, Association of Animal Behavior Professionals
32. Guy N. C.; Luescher U. A.; Dohoo S. E.; Spangler E.; Miller J. B; Dohoo I. R.; Bate L. A. (2001). "A case series of biting dogs: characteristics of the dogs, their behaviour, and their victims". Appl. Anim. Behav. Sci. 74: 15–57. doi:10.1016/S0168-1591(01)00155-1.
33. Takeuchi Y.; Ogata N.; Houpt J. A.; Scarlett J. M. (2001). "Differences in background and outcome of three behavior problems of dogs". Appl. Anim. Behav. Sci. 70 (4): 297–308. doi:10.1016/S0168-1591(00)00156-8. PMID 11179553.
34. Neilson J.; Eckstein R.; Hart B. (1997). "Effects on castration on problem behaviors in male dogs with reference to age and duration of behavior". JAVMA 211 (2): 180–182. PMID 9227747.
35. Polsky R. H. (1996). "Recognizing dominance aggression in dogs". Vet. Med. 91: 196–201.
36. Blackshaw, J.K. (1991). "An overview of types of aggressive behavior in dogs and methods of treatment". Appl. Anim. Behav. Sci. 30 (3–4): 351–361. doi:10.1016/0168-1591(91)90140-S.
37. Wright J. C. (1991). "Canine aggression toward people. Bite scenarios and prevention". Vet. Clin. North. Am. Small. Anim. Pract. 21 (2): 299–314. PMID 2053252.
38. Crowell-Davis S. L. (1991). "Identifying and correcting human-directed dominance aggression of dogs". Vet. Med. 86: 990–998.
39. Podberscek A. L.; Serpell J. A. (1996). "The English Cocker Spaniel: preliminary findings on aggressive behaviour". Appl. Anim. Behav. Sci. 47: 75–89. doi:10.1016/0168-1591(95)01012-2.
40. Meuten D. J. Tumors in Domestic Animals. 4th Edn. Iowa State Press, Blackwell Publishing Company, Ames, Iowa, p. 575
41. Spain C. V.; Scarlett J. M.; Houpt K. A. (2004). "Long-term risks and benefits of early-age gonadectomy in dogs". JAVMA 224 (3): 380–387. doi:10.2460/javma.2004.224.380. PMID 14765797.
42. Hooper R. N.; Taylor T. S.; Varner D. D.; Blanchard T. L. (October 1993). "Effects of bilateral ovariectomy via colpotomy in mares: 23 cases (1984–1990)". J. Am. Vet. Med. Assoc 203 (7): 1043–6. PMID 8226251.
43. Leoci, R.; Aiudi, G.; Silvestre, F.; Lacalandra, G. M. (September 2012). "Chemical sterilization with calcium chloride: a dose dependent study in the dog" and "Dog chemical castration by intratesticular injection of a calcium chloride in an alcohol solution". 1st International Conference on Dog Population Management.
44. Koger, L. M. (November 1977). "Calcium Chloride, Practical Necrotizing Agent". Journal of the American Association of Bovine Practitioners (USA) 12: 118–119.
45. "Neutersol and Esterilsol". acc-d.org. Alliance for Contraception in Cats and Dogs. Archived from the original on 31 December 2008. Retrieved 2008-11-28.
46. Matzuk, Martin M.; McKeown, Michael R.; Filippakopoulos, Panagis; Li, Qinglei; Ma, Lang; Agno, Julio E.; Lemieux, Madeleine E.; Picaud, Sarah; Yu, Richard N.; Qi, Jun; Knapp, Stefan; Bradner, James E. (2012-08-17). "Small-Molecule Inhibition of BRDT for Male Contraception". Cell 150 (4): 673–684. doi:10.1016/j.cell.2012.06.045. PMC 3420011. PMID 22901802.
47. Jones, Inke; Ricciardi, Lucas; Hall, Leonard; Hansen, Hedley; Varadan, Vijay; Bertram, Chris; Maddocks, Simon; Enderling, Stefan; Saint, David; Al-Sarawi, Said; Abbott, Derek (2008-01-17). "Wireless RF communication in biomedical applications" (pdf). Smart Materials and Structures (IOP Publishing Ltd) 17: 8–9. doi:10.1088/0964-1726/17/1/015050. Retrieved 2008-06-25.
48. SpayVac. Retrieved on early 2003.
49. Killian, Gary; Diehl, Nancy K.; Miller, Lowell; Rhyan, Jack; Thain, David (2007). "Long-term Efficacy of Three Contraceptive Approaches for Population Control of Wild Horses". Cattlemen's Update: 48–63.
50. DeNicola, Anthony; Miller, Lowell A.; Gionfriddo, James P.; Fagerstone, Kathleen A. (2007-03-16). "Status of Present Day Infertility Technology". Northeast Association of Fish and Wildlife Agencies. Archived from the original on 29 August 2007. Retrieved 2007-03-16.
51. Fried, N. M.; Sinelnikov, Y. D.; Pant, B. B.; Roberts, W. W.; Solomon, S. B. (December 2001). "Noninvasive vasectomy using a focused ultrasound clip: thermal measurements and simulations". Biomedical Engineering, IEEE Transactions on 48 (12): 1453–9. doi:10.1109/10.966604. PMID 11759926.
52. Smith, Lee B.; Milne, L.; Nelson, N.; Eddie, S.; Brown, P.; Atanassova, N.; O’Bryan, M. K.; O’Donnell, L.; Rhodes, D.; Wells, S.; Napper, D.; Nolan, P.; Lalanne, Z.; Cheeseman, M.; Peters, J. (May 2012). "KATNAL1 Regulation of Sertoli Cell Microtubule Dynamics is Essential for Spermiogenesis and Male Fertility". PLoS Genetics 8: e1002697. doi:10.1371/journal.pgen.1002697.
53. Jensen, Jeffrey T.; Zelinski, Mary B.; Stanley, Jessica E.; Fanton, John W.; Stouffer, Richard L. (April 2008). "The phosphodiesterase 3 inhibitor ORG 9935 inhibits oocyte maturation in the naturally selected dominant follicle in Rhesus macaques". Contraception 77 (4): 303–7. doi:10.1016/j.contraception.2008.01.003. PMC 2505347. PMID 18342656.
54. "Penectomized Teaser Bull". The Drost Project. Retrieved 2011-08-24.
55. Early-Age (Prepubertal) Spay/Neuter of Dogs and Cats
56. Early Neutering of Companion Animals Position Statement American Animal Hospital Association
57. Dog and Cat Spay/Castration at CanadianVeterinarians.net
58. Long-term risks and benefits of early-age gonadectomy in cats
59. Long-term risks and benefits of early-age gonadectomy in dogs
60. Howe, L. M.; Slater, M. R.; Boothe, H. W.; Hobson, H. P.; Fossum, T. W.; Spann, A. C.; Wilkie, W. S. (2000). "Long-term outcome of gonadectomy performed at an early age or traditional age in cats". Journal of the American Veterinary Medical Association 217 (11): 1661–5. doi:10.2460/javma.2000.217.1661. PMID 11110455.
61. Howe, Lisa M.; Slater, Margaret R.; Boothe, Harry W.; Hobson, H. Phil; Holcom, Jennifer L.; Spann, Angela C. (2001). "Long-term outcome of gonadectomy performed at an early age or traditional age in dogs". Journal of the American Veterinary Medical Association 218 (2): 217–21. doi:10.2460/javma.2001.218.217. PMID 11195826.
62. Howe (1997). "Short-term results and complications of prepubertal gonadectomy in cats and dogs". Journal of the American Veterinary Medical Association 211 (1): 57–62. PMID 9215412.
63. Kustritz, M. (2002). "Early spay-neuter: Clinical considerations". Clinical Techniques in Small Animal Practice 17 (3): 124–8. doi:10.1053/svms.2002.34328. PMID 12476815.
64. De Bleser, B.; Brodbelt, D. C.; Gregory, N. G.; Martinez, T. A. (2009). "The association between acquired urinary sphincter mechanism incompetence in bitches and early spaying: A case-control study". The Veterinary Journal 187 (1): 42–47. doi:10.1016/j.tvjl.2009.11.004. PMID 20004121.
65. Duerr; Duncan, C. G.; Savicky, R. S.; Park, R. D.; Egger, E. L.; Palmer, R. H. (2007). "Risk factors for excessive tibial plateau angle in large-breed dogs with cranial cruciate ligament disease". Journal of the American Veterinary Medical Association 231 (11): 1688–91. doi:10.2460/javma.231.11.1688. PMID 18052804.
66. http://www.vetmed.ucdavis.edu/faculty/results.cfm?fid=14642
67. http://grad-schools.usnews.rankingsandreviews.com/best-graduate-schools/top-health-schools/veterinarian-rankings
68. http://www.plosone.org/article/fetchObject.action?uri=info%3Adoi%2F10.1371%2Fjournal.pone.0055937&representation=PDF
69. http://www.plosone.org/article/fetchObject.action?uri=info%3Adoi%2F10.1371%2Fjournal.pone.0102241&representation=PDF
70. Islam Question and Answer – De-clawing a cat so that it won’t do any damage, and neutering/spaying cats
71. What some religions say about sterilisation.
72. http://www.spca.org.my/neuter.htm#5 Spaying/Neutering Information
73. What does Jewish law say about neutering male pets?
74. Feinstein, Moshe. Igrot Moshe.
75. CHAI – Why Spay/Neuter is Crucial

External links

• DVM Article on health effects of spay/neuter: Long-Term Health Risks and Benefits Associated with Spay / Neuter in Dogs
• Determining the optimal age for gonadectomy of dogs and cats (pdf)
• Canine Spay Photos and Description
• Educational campaign about spaying/neutering pets at 4 months of age